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Journal of Clinical Oncology, Vol 22, No 6 (March 15), 2004: pp. 1103-1109
© 2004 American Society of Clinical Oncology.
DOI: 10.1200/JCO.2004.08.158
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Bronchioloalveolar Pathologic Subtype and Smoking History Predict Sensitivity to Gefitinib in Advanced Non–Small-Cell Lung Cancer

Vincent A. Miller, Mark G. Kris, Neelam Shah, Jyoti Patel, Christopher Azzoli, Jorge Gomez, Lee M. Krug, William Pao, Naiyer Rizvi, Barbara Pizzo, Leslie Tyson, Ennapadam Venkatraman, Leah Ben-Porat, Natalie Memoli, Maureen Zakowski, Valerie Rusch, Robert T. Heelan

From the Thoracic Oncology Service, Departments of Medicine, Biostatistics, Pathology, Surgery, and Radiology, Memorial Sloan-Kettering Cancer Center, New York, NY.

Address reprint requests to Vincent A. Miller, MD, Thoracic Oncology Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021; e-mail: millerv{at}mskcc.org

PURPOSE: Gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, induces radiographic regressions and symptomatic improvement in patients with non–small-cell lung cancer (NSCLC). Phase II trials suggested female sex and adenocarcinoma were associated with response. We undertook this analysis to identify additional clinical and pathologic features associated with sensitivity to gefitinib.

PATIENTS AND METHODS: We reviewed medical records, pathologic material, and imaging studies of all 139 NSCLC patients treated on one of three consecutive studies of gefitinib monotherapy performed at our institution. We identified patients experiencing a major objective response and compared their clinical and pathologic features with the others. Univariate and multivariable analyses were performed on potential predictive features associated with sensitivity to gefitinib.

RESULTS: Of 139 patients, 21 (15%; 95% CI, 9% to 21%), experienced a partial radiographic response. Variables identified as significant in univariate analysis included adenocarcinoma versus other NSCLC (19% v 0%; P = .004), adenocarcinoma with bronchioloalveolar features versus other adenocarcinomas (38% v 14%; P < .001), never smoker status versus former/current (36% v 8%; P < .001), and Karnofsky performance status >= 80% versus <= 70% (22% v 8%; P = .03). Multivariable analysis revealed the presence of adenocarcinoma with any bronchioloalveolar features (P = .004) and being a never smoker (P = .006) were independent predictors of response.

CONCLUSION: Our data suggest that individuals in whom gefitinib is efficacious are more likely to have adenocarcinomas of the bronchioloalveolar subtype and to be never smokers. These observations may provide clues to mechanisms determining sensitivity to this agent and suggest that NSCLC has a different biology in patients who never smoked and those with bronchioloalveolar carcinoma.

Supported in part by AstraZeneca, Wilmington, DE.

Presented in part at the 39th Annual Meeting of the American Society of Clinical Oncology, Chicago, IL, May 31-June 3, 2003, and the 10th World Conference on Lung Cancer, Vancouver, British Columbia, Canada, Aug 10-14, 2003.

Authors' disclosures of potential conflicts of interest are found at the end of this article.


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Role of Chemotherapy and the Receptor Tyrosine Kinases KIT, PDGFR{alpha}, PDGFR{beta}, and Met in Large-Cell Neuroendocrine Carcinoma of the Lung
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E. B. Haura, Z. Zheng, L. Song, A. Cantor, and G. Bepler
Activated Epidermal Growth Factor Receptor-Stat-3 Signaling Promotes Tumor Survival In vivo in Non-Small Cell Lung Cancer
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J. A. Zell, S.-H. I. Ou, A. Ziogas, and H. Anton-Culver
Epidemiology of Bronchioloalveolar Carcinoma: Improvement in Survival After Release of the 1999 WHO Classification of Lung Tumors
J. Clin. Oncol., November 20, 2005; 23(33): 8396 - 8405.
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C. Ho, J. Davis, F. Anderson, G. Bebb, and N. Murray
Side Effects Related to Cancer Treatment: CASE 1. Hepatitis Following Treatment With Gefitinib
J. Clin. Oncol., November 20, 2005; 23(33): 8531 - 8533.
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I. K. Mellinghoff, M. Y. Wang, I. Vivanco, D. A. Haas-Kogan, S. Zhu, E. Q. Dia, K. V. Lu, K. Yoshimoto, J. H.Y. Huang, D. J. Chute, et al.
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N. Ishikawa, Y. Daigo, A. Takano, M. Taniwaki, T. Kato, S. Hayama, H. Murakami, Y. Takeshima, K. Inai, H. Nishimura, et al.
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F. R. Hirsch, M. Varella-Garcia, J. McCoy, H. West, A. C. Xavier, P. Gumerlock, P. A. Bunn Jr, W. A. Franklin, J. Crowley, and D. R. Gandara
Increased Epidermal Growth Factor Receptor Gene Copy Number Detected by Fluorescence In Situ Hybridization Associates With Increased Sensitivity to Gefitinib in Patients With Bronchioloalveolar Carcinoma Subtypes: A Southwest Oncology Group Study
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M. G. Kris
How Today's Developments in the Treatment of Non-Small Cell Lung Cancer Will Change Tomorrow's Standards of Care
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W. P. Tew, D. P. Kelsen, and D. H. Ilson
Targeted Therapies for Esophageal Cancer
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L. V. Sequist, D. A. Haber, and T. J. Lynch
Epidermal Growth Factor Receptor Mutations in Non-Small Cell Lung Cancer: Predicting Clinical Response to Kinase Inhibitors
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F. Cappuzzo, M. Varella-Garcia, H. Shigematsu, I. Domenichini, S. Bartolini, G. L. Ceresoli, E. Rossi, V. Ludovini, V. Gregorc, L. Toschi, et al.
Increased HER2 Gene Copy Number Is Associated With Response to Gefitinib Therapy in Epidermal Growth Factor Receptor-Positive Non-Small-Cell Lung Cancer Patients
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Q. Pan, W. Pao, and M. Ladanyi
Rapid Polymerase Chain Reaction-Based Detection of Epidermal Growth Factor Receptor Gene Mutations in Lung Adenocarcinomas
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F. A. Shepherd, J. Rodrigues Pereira, T. Ciuleanu, E. H. Tan, V. Hirsh, S. Thongprasert, D. Campos, S. Maoleekoonpiroj, M. Smylie, R. Martins, et al.
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M. S. Tsao, A. Sakurada, J.-C. Cutz, C.-Q. Zhu, S. Kamel-Reid, J. Squire, I. Lorimer, T. Zhang, N. Liu, M. Daneshmand, et al.
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Z. Zheng, G. Bepler, A. Cantor, and E. B. Haura
Small Tumor Size and Limited Smoking History Predicts Activated Epidermal Growth Factor Receptor in Early-Stage Non-small Cell Lung Cancer
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R.-K. Hsieh, K.-H. Lim, H.-T. Kuo, C.-Y. Tzen, and M.-J. Huang
Female Sex and Bronchioloalveolar Pathologic Subtype Predict EGFR Mutations in Non-small Cell Lung Cancer
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Gefitinib-Sensitive Mutations of the Epidermal Growth Factor Receptor Tyrosine Kinase Domain in Chinese Patients with Non-Small Cell Lung Cancer
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O. Altundag, K. Altundag, P. Morandi, and M. Gunduz
Association Between Epidermal Growth Factor Receptor Mutation and Improved Survival in Never-Smokers With Primary Adenocarcinoma of the Lung
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Mutation in the Tyrosine Kinase Domain of Epidermal Growth Factor Receptor Is a Predictive and Prognostic Factor for Gefitinib Treatment in Patients with Non-Small Cell Lung Cancer
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P. A. Janne, J. A. Engelman, and B. E. Johnson
Epidermal Growth Factor Receptor Mutations in Non-Small-Cell Lung Cancer: Implications for Treatment and Tumor Biology
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G. Giaccone
Epidermal Growth Factor Receptor Inhibitors in the Treatment of Non-Small-Cell Lung Cancer
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K. M.W. Pisters and T. Le Chevalier
Adjuvant Chemotherapy in Completely Resected Non-Small-Cell Lung Cancer
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W. D. Travis, K. Garg, W. A. Franklin, I. I. Wistuba, B. Sabloff, M. Noguchi, R. Kakinuma, M. Zakowski, M. Ginsberg, R. Padera, et al.
Evolving Concepts in the Pathology and Computed Tomography Imaging of Lung Adenocarcinoma and Bronchioloalveolar Carcinoma
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V. A. Miller, F. R. Hirsch, and D. H. Johnson
Systemic Therapy of Advanced Bronchioloalveolar Cell Carcinoma: Challenges and Opportunities
J. Clin. Oncol., May 10, 2005; 23(14): 3288 - 3293.
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F. Cappuzzo, F. R. Hirsch, E. Rossi, S. Bartolini, G. L. Ceresoli, L. Bemis, J. Haney, S. Witta, K. Danenberg, I. Domenichini, et al.
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M. K. Mohamed, S. Ramalingam, Y. Lin, W. Gooding, and C. P. Belani
Skin rash and good performance status predict improved survival with gefitinib in patients with advanced non-small cell lung cancer
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D. H. Lee, J.-Y. Han, H. G. Lee, J. J. Lee, E. K. Lee, H. Y. Kim, H. K. Kim, E. K. Hong, and J. S. Lee
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S.-W. Han, T.-Y. Kim, P. G. Hwang, S. Jeong, J. Kim, I. S. Choi, D.-Y. Oh, J. H. Kim, D.-W. Kim, D. H. Chung, et al.
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J. Baselga and C. L. Arteaga
Critical Update and Emerging Trends in Epidermal Growth Factor Receptor Targeting in Cancer
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W. Pao and V. A. Miller
Epidermal Growth Factor Receptor Mutations, Small-Molecule Kinase Inhibitors, and Non-Small-Cell Lung Cancer: Current Knowledge and Future Directions
J. Clin. Oncol., April 10, 2005; 23(11): 2556 - 2568.
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G. Giaccone
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A. J. Mantha, J. E.L. Hanson, G. Goss, A. E. Lagarde, I. A. Lorimer, and J. Dimitroulakos
Targeting the Mevalonate Pathway Inhibits the Function of the Epidermal Growth Factor Receptor
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S. Kobayashi, T. J. Boggon, T. Dayaram, P. A. Janne, O. Kocher, M. Meyerson, B. E. Johnson, M. J. Eck, D. G. Tenen, and B. Halmos
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L. P. Stabile, J. S. Lyker, C. T. Gubish, W. Zhang, J. R. Grandis, and J. M. Siegfried
Combined Targeting of the Estrogen Receptor and the Epidermal Growth Factor Receptor in Non-Small Cell Lung Cancer Shows Enhanced Antiproliferative Effects
Cancer Res., February 15, 2005; 65(4): 1459 - 1470.
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A. Marchetti, C. Martella, L. Felicioni, F. Barassi, S. Salvatore, A. Chella, P. P. Camplese, T. Iarussi, F. Mucilli, A. Mezzetti, et al.
EGFR Mutations in Non-Small-Cell Lung Cancer: Analysis of a Large Series of Cases and Development of a Rapid and Sensitive Method for Diagnostic Screening With Potential Implications on Pharmacologic Treatment
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